Heterogeneity in resistance to food-related stresses and biofilm formation ability among verocytotoxigenic Escherichia coli strains

International Journal of Food Microbiology

Volumn 161, Issue 3, 2013, Pages 220-230

  Alvarez Ordonez A ^a   Alvseike, O ^b   Omer, M K ^b   Heir, E ^c   Axelsson, L ^c   Holck, A ^c   Prieto, M ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b Animalia   (Norway)

^c NOFIMA   (Norway)

Author keywords

Biofilms; Fourier Transform Infrared spectroscopy; RpoS; Stress tolerance; VTEC

Indexed keywords

ACID; SIGMA FACTOR RPOS; SORBITOL;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; BIOFILM; CELL COMPOSITION; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL STRESS; ESCHERICHIA COLI; FERMENTATION; HEAT; HYDROSTATIC PRESSURE; INFRARED SPECTROSCOPY; LOSS OF FUNCTION MUTATION; VEROCYTOTOXIGENIC ESCHERICHIA COLI;

EID: 84872662889     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2012.12.008     Document Type: Article

References (87)

1. Adams J.L., McLean R.J.C. Impact of rpoS deletion on Escherichia coli biofilms. Applied and Environmental Microbiology 1999, 65:4285-4287.
2. Alpas H., Kalchayanand N., Bozoglu F., Sikes A., Dunne C.P., Ray B. Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Applied and Environmental Microbiology 1999, 65:4248-4251.
3. Al-Qadiri H.M., Lin M., Cavinato A.G., Rasco B.A. Fourier transform infrared spectroscopy, detection and identification of Escherichia coli O157:H7 and Alicyclobacillus strains in apple juice. International Journal of Food Microbiology 2006, 111:73-80.
4. Al-Qadiri H.M., Al-Alami N.I., Al-Holy M.A., Rasco B.A. Using Fourier transform infrared (FT-IR) absorbance spectroscopy and multivariate analysis to study the effect of chlorine-induced bacterial injury in water. Journal of Agricultural and Food Chemistry 2008, 56:8992-8997.
5. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997, 25:3389-3402.
6. Álvarez I., Mañas P., Condón S., Raso J. Resistance variation of Salmonella enterica serovars to pulsed electric fields treatments. Journal of Food Science 2003, 68:2316-2320.
7. Álvarez-Ordóñez A., Prieto M. Changes in ultrastructure and Fourier transform infrared spectrum of Salmonella enterica serovar Typhimurium cells after exposure to stress conditions. Applied and Environmental Microbiology 2010, 76:7598-7607.
8. Álvarez-Ordóñez A., Prieto M. Fourier transform infrared spectroscopy in food microbiology. SpringerBriefs in Food, Health, and Nutrition 2012, 10.1007/978-1-4614-3813-7.
9. Álvarez-Ordóñez A., Mouwen D.J.M., López M., Prieto M. Fourier transform infrared spectroscopy as a tool to characterize molecular composition and stress response in foodborne pathogenic bacteria. Journal of Microbiological Methods 2011, 84:369-378.
10. Álvarez-Ordóñez A., Begley M., Hill C. Polymorphisms in rpoS and heterogeneity in stress tolerance in natural isolates of Cronobacter sakazakii. Applied and Environmental Microbiology 2012, 78:3975-3984.
11. Arnold K.W., Kaspar C.W. Starvation- and stationary-phase-induced acid tolerance in Escherichia coli O157:H7. Applied and Environmental Microbiology 1995, 61:2037-2039.
12. Benito A., Ventoura G., Casadei M., Robinson T., Mackey B. Variation in resistance of natural isolates of Escherichia coli O157 to high hydrostatic pressure, mild heat and other stresses. Applied and Environmental Microbiology 1999, 65:1564-1569.
13. Benjamin M.M., Datta A.R. Acid tolerance of enterohemorrhagic Escherichia coli. Applied and Environmental Microbiology 1995, 61:1669-1672.
14. Bergholz T.M., Whittam T.S. Variation in acid resistance among enterohaemorrhagic Escherichia coli in a simulated gastric environment. Journal of Applied Microbiology 2006, 102:352-362.
15. Berry E.D., Barkocy-Gallagher G.A., Siragusa G.R. Stationary-phase acid resistance and injury of recent bovine Escherichia coli O157 and non-O157 biotype I Escherichia coli isolates. Journal of Food Protection 2004, 67:583-590.
16. Bettelheim K.A., Whipp M., Djordjevic S.P., Ramachandran V. First isolation outside Europe of sorbitol-fermenting verocytotoxigenic Escherichia coli (VTEC) belonging to O group O157. Journal of Medical Microbiology 2002, 51:713-714.
17. Bhagwat A.A., Chan L., Han R., Tan J., Kothary M., Jean-Gilles J., Tall B.D. Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infection and Immunity 2005, 73:4993-5003.
18. Bhagwat A.A., Tan J., Sharma M., Kothary M., Low S., Tall B.D., Bhagwat M. Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Applied and Environmental Microbiology 2006, 72:4978-4986.
19. Bielaszewska M., Mellmann A., Zhang W., Köck R., Fruth A., Bauwens A., Peters G., Karch H. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany 2011: a microbiological study. The Lancet Infectious Diseases 2011, 11:671-676.
20. Brown J., Ross T., McMeekin T., Nichols P. Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. International Journal of Food Microbiology 1997, 37:163-173.
21. Buchanan R.L., Edelson S.G. pH-dependent stationary-phase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants. Journal of Food Protection 1999, 62:211-218.
22. CDC Laboratory-confirmed non-O157 Shiga toxin-producing Escherichia coli - Connecticut, 2001-2005. Morbidity and Mortality Weekly Report 2007, 56:29-31.
23. Choi S.H., Baumler D.J., Kaspar C.W. Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Applied and Environmental Microbiology 2000, 66:3911-3916.
24. Conesa R., Andreu S., Fernández P.S., Esnoz A., Palop A. Nonisothermal heat resistance determinations with the thermoresistometer Mastia. Journal of Applied Microbiology 2009, 107:506-513.
25. Culham D.E., Wood J.M. An Escherichia coli reference collection group B2- and uropathogen-associated polymorphism in the rpoS-mutS region of the E. coli chromosome. Journal of Bacteriology 2000, 182:6272-6276.
26. Djordjevic D., Wiedmann M., McLandsborough L.A. Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Applied and Environmental Microbiology 2002, 68:2950-2958.
27. Dodd C.E.R., Aldsworth T.G. The importance of RpoS in the survival of bacteria through food processing. International Journal of Food Microbiology 2002, 74:189-194.
28. Enache E., Mathusa E.C., Elliot P.H., Glenn Black D., Chen Y., Scott V.N., Schaffner D.W. Thermal resistance parameters for shiga toxin-producing Escherichia coli in apple juice. Journal of Food Protection 2011, 74:1231-1237.
29. European Food Safety Authority (EFSA) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 2012, 10:2597.
30. Ferenci T. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli?. Trends in Microbiology 2003, 11:457-461.
31. Ferenci T. The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype of the fixation of rpoS mutations. Heredity 2008, 100:446-452.
32. Fernández A., Álvarez-Ordóñez A., López M., Bernardo A. Effects of organic acids on thermal inactivation of acid and cold stressed Enterococcus faecium. Food Microbiology 2009, 26:497-503.
33. Foster J.W. Microbial responses to acid stress. Bacterial Stress Responses 2000, 99-115. ASM Press, Washington DC, USA. G. Storz, R. Hengge-Aronis (Eds.).
34. Foster J.W. Escherichia coli acid resistance: tales of an amateur acidophile. Nature Reviews Microbiology 2004, 2:898-907.
35. Gyles C.L. Shiga toxin-producing Escherichia coli: an overview. Journal of Animal Science 2007, 85:E45-E62.
36. Habimana O., Heir E., Wold Åsli A., Langsrud S., Møretrø T. Enhanced surface colonization by Escherichia coli O157:H7 in biofilms formed by an Acinetobacter calcoaceticus isolate from meat-processing environment. Applied and Environmental Microbiology 2010, 76:4557-4559.
37. Hauben K.J.A., Bartlett D.H., Soontjens C.C.F., Cornelis K., Wuytack E.Y., Michiels C.W. Escherichia coli mutants resistant to inactivation by high hydrostatic pressure. Applied and Environmental Microbiology 1997, 63:945-950.
38. Heir E., Holck A.L., Omer M.K., Alvseike O., Hoy M., Mage I., Axelsson L. Reduction of verotoxigenic Escherichia coli by process and recipe optimisation in dry-fermented sausages. International Journal of Food Microbiology 2010, 141:195-202.
39. Hengge-Aronis R. The general stress response in Escherichia coli. Bacterial Stress Responses 2000, 161-178. ASM Press, Washington DC, USA. G. Storz, R. Hengge-Aronis (Eds.).
40. Hu X., Qiu Z., Wang Y., She Z., Qian G., Ren Z. Effect of ultra-strong static magnetic field on bacteria: application of Fourier-transform infrared spectroscopy combined with cluster analysis and deconvolution. Bioelectromagnetics 2009, 30:500-507.
41. Humphrey T.J., Slater E., McAlpine K., Rowbury R.J., Gilbert R. Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid or hydrogen peroxide also survive longer on surfaces. Applied and Environmental Microbiology 1995, 61:3161-3164.
42. Ito A., May T., Kawata K., Okabe S. Significance of rpoS during maturation of Escherichia coli biofilms. Biotechnology and Bioengineering 2008, 99:1462-1471.
43. Iyer R., Williams C., Miller C. Arginine-agmatine antiporter in extreme acid resistance in Escherichia coli. Journal of Bacteriology 2003, 185:6556-6561.
44. Jenke C., Harmsen D., Weniger T., Rothgänger J., Hyytiä-Trees E., Bielaszewska M., Karch H., Mellmann A. Phylogenetic analysis of enterohemorrhagic Escherichia coli O157, Germany, 1987-2008. Emerging Infectious Diseases 2010, 16:610-616.
45. Jeong K.C., Hung K.F., Baumler D.J., Byrd J.J., Kaspar C.W. Acid stress damage of DNA is prevented by Dps binding in Escherichia coli O157:H7. BMC Microbiology 2008, 8:181. (15).
46. Juneja V.K., Marks H.M. Heat resistance kinetics variation among various isolates of Escherichia coli. Innovative Food Science and Emerging Technologies 2005, 6:155-161.
47. Karch H., Bielaszewska M. Sorbitol-fermenting Shiga-toxin-producing Escherichia coli O157:H(-) strains: epidemiology, phenotypic and molecular characteristics, and microbiological diagnosis. Journal of Clinical Microbiology 2001, 39:2043-2049.
48. King T., Ishihama A., Kori A., Ferenci T. A regulatory trade-off as a source of strain variation in the species Escherichia coli. Journal of Bacteriology 2004, 186:5614-5620.
49. Klotz B., Pyle D.L., Mackey B.M. New mathematical modeling approach for predicting microbial inactivation by high hydrostatic pressure. Applied and Environmental Microbiology 2007, 73:2468-2478.
50. Kumar C.G., Anand S.K. Significance of microbial biofilms in food industry: a review. International Journal of Food Microbiology 1998, 42:9-27.
51. L'Abée-Lund T.M., Jørgensen H.J., O'Sullivan K., Bohlin J., Ligård G., Granum P.E., Lindbäck T. The highly virulent 2006 Norwegian EHEC O103:H25 outbreak strain is related to the 2011 German O104:H4 outbreak strain. PLoS One 2012, 7:e31413.
52. Large T.M., Walk S.T., Whittam T.S. Variation in acid resistance among shiga toxin-producing clones of pathogenic Escherichia coli. Applied and Environmental Microbiology 2005, 71:2493-2500.
53. Leyer G.J., Wang L.L., Johnson E.A. Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Applied and Environmental Microbiology 1995, 61:3752-3755.
54. Lin J., Smith M.P., Chapin K.C., Baik H.S., Bennett G.N., Foster J.W. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Applied and Environmental Microbiology 1996, 62:3094-3100.
55. Lindstedt B.A., Brandal L.T., Aas L., Vardund T., Kapperud G. Study of polymorphic variable-number of tandem repeats loci in the ECOR collection and in a set of pathogenic Escherichia coli and Shigella isolates for use in a genotyping assay. Journal of Microbiological Methods 2007, 69:197-205.
56. Mafart P., Couvert O., Gaillard S., Leguerinel I. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. International Journal of Food Microbiology 2002, 72:107-113.
57. Manning S.D., Madera R.T., Schneider W., Dietrich S.E., Khalife W., Brown W., Whittam T.S., Somsel P., Rudrick J.T. Surveillance for shiga-toxin producing Escherichia coli, Michigan, 2001-2005. Emerging Infectious Diseases 2007, 13:318-321.
58. McKellar R.C., Knight K.P. Growth and survival of various strains of enterohemorrhagic Escherichia coli in hydrochloric and acetic acid. Journal of Food Protection 1999, 62:1466-1469.
59. Møretrø T., Heir E., Mo K.R., Habimana O., Abdelgani A., Langsrud S. Factors affecting survival of Shigatoxin-producing Escherichia coli on abiotic surfaces. International Journal of Food Microbiology 2010, 138:71-77.
60. Mouwen D.J.M., Weijtens M.J.B.M., Capita R., Alonso-Calleja C., Prieto M. Discrimination of enterobacterial repetitive intergenic consensus PCR types of Campylobacter coli and Campylobacter jejuni by Fourier Transform infrared spectroscopy. Applied and Environmental Microbiology 2005, 71:4318-4324.
61. Murinda S.E., Nguyen L.T., Landers T.L., Draughon F.A., Mathew A.G., Hogan J.S., Smith K.L., Hancock D.D., Oliver S.P. Comparison of Escherichia coli isolates from humans, food, and farm and companion animals for presence of Shiga toxin-producing E. coli virulence markers. Foodborne Pathogens and Disease 2004, 1:178-184.
62. Naumann D. Infrared spectroscopy in microbiology. Encyclopedia of Analytical Chemistry 2000, 102-131. John Wiley & Sons Ltd., Chichester, UK. R.A. Meyers (Ed.).
63. Notley-McRobb L., King T., Ferenci T. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. Journal of Bacteriology 2002, 184:806-811.
64. Paton A., Ratcliff R., Doyle R., Seymour-Murray J., Davos D., Lanser J., Paton J. Molecular microbiological investigation of an outbreak of hemolytic-uremic syndrome caused by dry fermented sausage contaminated with shiga-like toxin-producing Escherichia coli. Journal of Clinical Microbiology 1996, 34:1622-1627.
65. Possé B., De Zutter L., Heyndrickx M., Herman L. Metabolic and genetic profiling of clinical O157 and non-O157 Shiga-toxin-producing Escherichia coli. Research in Microbiology 2007, 158:591-599.
66. Prager R., Annemüller S., Tschäpe H. Diversity of virulence patterns among shiga toxin-producing Escherichia coli from human clinical cases - need for more detailed diagnostics. International Journal of Medical Microbiology 2005, 295:29-38.
67. Rendueles E., Omer K.H., Alvseike O., Capita R., Alonso-Calleja C., Prieto M. Microbiological safety assessment in high hydrostatic pressure processing. LWT- Food Science and Technology 2011, 44:1251-1260.
68. Rhoades J.R., Duffy G., Koutsoumanis K. Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: a review. Food Microbiology 2009, 26:357-376.
69. Richard H., Foster J.W. Escherichia coli glutamate and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. Journal of Bacteriology 2004, 186:6032-6041.
70. Riley L.W., Remis R.S., Helgerson S.D., McGee H.B., Wells J.G., Davis B.R., Hebert R.J., Olcott E.S., Johnson L.M., Hargrett N.T., Blake P.A., Cohen M.L. Hemorrhagic colitis associated with a rare Escherichia coli serotype. The New England Journal of Medicine 1983, 308:681-685.
71. Robey M., Benito A., Hutson R.H., Pascual C., Park S.F., Mackey B.M. Variation in resistance to high hydrostatic pressure and rpoS heterogeneity in natural isolates of Escherichia coli O157:H7. Applied and Environmental Microbiology 2001, 67:4901-4907.
72. Rodríguez-Calleja J.M., Cebrián G., Condón S., Mañas P. Variation in resistance of natural isolates of Staphylococcus aureus to heat, pulsed electric field and ultrasound under pressure. Journal of Applied Microbiology 2006, 100:1054-1062.
73. Rowe M.T., Kirk R.B. Effect of nutrient starvation on the resistance of Escherichia coli O157:H7 to subsequent heat stress. Journal of Food Protection 2000, 63:1745-1748.
74. Sartz L., De Jong B., Hjertqvist M., Plym-Forshell L., Alsterlund R., Lofdahl S., Osterman B., Stahl A., Eriksson E., Hansson H., Karpman D. An outbreak of Escherichia coli O157:H7 infection in southern Sweden associated with consumption of fermented sausage; aspects of sausage production that increase the risk of contamination. Epidemiology and Infection 2008, 136:370-380.
75. Schembri M.A., Kjaergaard K., Klemm P. Global gene expression in Escherichia coli biofilms. Molecular Microbiology 2003, 48:253-267.
76. Scheutz F., Nielsen E., Frimodt-Møller J., Boisen N., Morabito S., Tozzoli R., Nataro J.P., Caprioli A. Characteristics of the enteroaggregative shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Eurosurveillance 2011, 16(24).
77. Schimmer B., Nygard K., Eriksen H.-M., Lassen J., Lindstedt B.-A., Brandal L., Kapperud G., Aavitsland P. Outbreak of haemolytic uraemic syndrome in Norway caused by stx2-positive Escherichia coli O103:H25 traced to cured mutton sausages. BMC Infectious Diseases 2008, 8:41.
78. Sherry A.E., Patterson M.F., Madden R.H. Comparison of 40 Salmonella enterica serovars injured by thermal, high-pressure and irradiation stress. Journal of Applied Microbiology 2004, 96:887-893.
79. Somolinos M., García D., Mañas P., Condón S., Pagán R. Effect of environmental factors and cell physiological state on pulsed electric fields resistance and repair capacity of various strains of Escherichia coli. International Journal of Food Microbiology 2008, 124:260-267.
80. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22:4673-4680.
81. Uhlich G.A., Sinclair J.R., Warren N.G., Chmielecki W.A., Fratamico P. Characterization of shiga toxin-producing Escherichia coli isolates associated with two multistate food-borne outbreaks that occurred in 2006. Applied and Environmental Microbiology 2008, 74:1268-1272.
82. Waterman S.R., Small P.L.C. Characterization of the acid resistance phenotype and rpoS alleles of shiga-like toxin-producing Escherichia coli. Infection and Immunity 1996, 64:2808-2811.
83. Weber H., Polen T., Heuveling J., Wendisch V.F., Hengge R. Genome-wide analysis of the general stress response network in Escherichia coli: sigma(S)-dependent genes, promoters, and sigma factor selectivity. Journal of Bacteriology 2005, 187:1591-1603.
84. Whiting R.C., Golden M.H. Variation among Escherichia coli O157:H7 strains relative to their growth, survival, thermal inactivation, and toxin production in broth. International Journal of Food Microbiology 2002, 75:127-133.
85. Whitney B.M., Williams R.C., Eifert J., Marcy J. High-pressure resistance variation of Escherichia coli O157:H7 strains and Salmonella serovars in tryptic soy broth, distilled water, and fruit juice. Journal of Food Protection 2007, 70:2078-2083.
86. Yuk H.G., Marshall D.L. Adaptation of Escherichia coli O157:H7 to pH alters membrane lipid composition, verotoxin secretion, and resistance to simulated gastric fluid acid. Applied and Environmental Microbiology 2004, 70:3500-3505.
87. Yuk H.G., Marshall D.L. Influence of acetic, citric, and lactic acids on Escherichia coli O157:H7 membrane lipid composition, verotoxin secretion, and acid resistance in simulated gastric fluid. Journal of Food Protection 2005, 68:673-679.